Targeting nodal in conjunction with dacarbazine induces synergistic anticancer effects in metastatic melanoma

Molecular Cancer Research

Volumn 13, Issue 4, 2015, Pages 670-680

  Hardy, Katharine M ^a   Strizzi, Luigi ^a   Margaryan, Naira V ^a   Gupta, Kanika ^a,b   Murphy, George F ^c   Scolyer, Richard A ^d,e   Hendrix, Mary J C ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d UNIVERSITY OF SYDNEY   (Australia)

^e ROYAL PRINCE ALFRED HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DACARBAZINE; PROTEIN ANTIBODY; PROTEIN NODAL; ANTINEOPLASTIC ANTIBIOTIC; NODAL PROTEIN, HUMAN;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENTIATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; METASTATIC MELANOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; TUMOR INVASION; APOPTOSIS; CELL PROLIFERATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; IMMUNOLOGY; MELANOMA; METABOLISM; METASTASIS; MOLECULARLY TARGETED THERAPY; SKIN NEOPLASMS; TUMOR CELL LINE;

ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; DACARBAZINE; DRUG SYNERGISM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MELANOMA; MOLECULAR TARGETED THERAPY; NEOPLASM METASTASIS; NODAL PROTEIN; SKIN NEOPLASMS;

EID: 84928042291     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-14-0077     Document Type: Article

References (49)

1. Gogas HJ, Kirkwood JM, Sondak VK. Chemotherapy for metastatic melanoma: time for a change? Cancer 2007;109:455-64.
2. Serrone L, ZeuliM, Sega FM, Cognetti F. Dacarbazine-based chemotherapy for metastatic melanoma: thirty-year experience overview. J Exp Clin Cancer Res 2000;19:21-34.
3. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 2011;364:2507-16.
4. Hauschild A, Grob JJ, Demidov LV, Jouary T, Gutzmer R, Millward M, et al. Dabrafenib in BRAF-mutated metastatic melanoma: a multicentre, open-label, phase 3 randomised controlled trial. Lancet 2012; 380:358-65.
5. Flaherty KT, Robert C, Hersey P, Nathan P, Garbe C, Milhem M, et al. Improved survival with MEK inhibition in BRAF-mutated melanoma. N Engl J Med 2012;367:107-14.
6. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
7. Robert C, Ribas A, Wolchok JD, Hodi FS, Hamid O, Kefford R, et al. Anti-programmed-death-receptor-1 treatment with pembrolizumab in ipilimumab-refractory advanced melanoma: a randomised dose-comparison cohort of a phase 1 trial. Lancet 2014;384:1109-17.
8. Kirkwood JM, Strawderman MH, Ernstoff MS, Smith TJ, Borden EC, Blum RH. Interferon alfa-2b adjuvant therapy of high-risk resected cutaneous melanoma: the Eastern Cooperative OncologyGroup Trial EST 1684. JClin Oncol 1996;14:7-17.
9. Atkins MB, Lotze MT, Dutcher JP, Fisher RI,Weiss G, Margolin K, et al. Highdose recombinant interleukin 2 therapy for patients with metastatic melanoma: analysis of 270 patients treated between 1985 and 1993. J Clin Oncol 1999;17:2105-16.
10. Sullivan RJ, Flaherty KT. Resistance to BRAF-targeted therapy inmelanoma. Eur J Cancer 2013;49:1297-304.
11. Sullivan RJ, Lorusso PM, Flaherty KT. The intersection of immune-directed and molecularly targeted therapy in advanced melanoma: where we have been, are, and will be. Clin Cancer Res 2013;19:5283-91.
12. Eggermont AM, Kirkwood JM. Re-evaluating the role of dacarbazine in metastatic melanoma: what have we learned in 30 years? Eur J Cancer 2004;40:1825-36.
13. Mouawad R, Sebert M,Michels J, Bloch J, Spano JP, Khayat D. Treatment for metastatic malignant melanoma: old drugs and new strategies. Crit Rev Oncol Hematol 2010;74:27-39.
14. Kwong LN, Davies MA. Targeted therapy for melanoma: rational combinatorial approaches. Oncogene 2014;33:1-9.
15. Shen MM. Nodal signaling: developmental roles and regulation. Development 2007;134:1023-34.
16. Schier AF. Nodal morphogens. Cold Spring Harb Perspect Biol 2009;1: a003459.
17. Quail DF, Siegers GM, Jewer M, Postovit LM. Nodal signalling in embryogenesis and tumourigenesis. Int J Biochem Cell Biol 2013;45:885-98.
18. Topczewska JM, Postovit LM, Margaryan NV, Sam A, Hess AR, Wheaton WW, et al. Embryonic and tumorigenic pathways converge via Nodal signaling: role in melanoma aggressiveness. Nat Med 2006;12: 925-32.
19. Postovit LM, Margaryan NV, Seftor EA, Kirschmann DA, Lipavsky A, Wheaton WW, et al. Human embryonic stem cell microenvironment suppresses the tumorigenic phenotype of aggressive cancer cells. Proc Natl Acad Sci U S A 2008;105:4329-34.
20. Papageorgiou I, Nicholls PK, Wang F, Lackmann M, Makanji Y, Salamonsen LA, et al. Expression of nodal signalling components in cycling human endometrium and in endometrial cancer. Reprod Biol Endocrinol 2009; 7:122.
21. Hardy KM, Kirschmann DA, Seftor EA, Margaryan NV, Postovit LM, Strizzi L, et al. Regulation of the embryonic morphogen Nodal by Notch4 facilitates manifestation of the aggressive melanoma phenotype. Cancer Res 2010;70:10340-50.
22. Lawrence MG, Margaryan NV, Loessner D, Collins A, Kerr KM, Turner M, et al. Reactivation of embryonic nodal signaling is associated with tumor progression and promotes the growth of prostate cancer cells. Prostate 2011;71:1198-209.
23. Strizzi L, Hardy KM, Margaryan NV, Hillman DW, Seftor EA, Chen B, et al. Potential for the embryonic morphogen Nodal as a prognostic and predictive biomarker in breast cancer. Breast Cancer Res 2012;14:R75.
24. Costa FF, Seftor EA, Bischof JM, Kirschmann DA, Strizzi L, Arndt K, et al. Epigenetically reprogramming metastatic tumor cells with an embryonic microenvironment. Epigenomics 2009;1:387-98.
25. Strizzi L, Postovit LM, Margaryan NV, Lipavsky A, Gadiot J, Blank C, et al. Nodal as a biomarker for melanoma progression and a new therapeutic target for clinical intervention. Expert Rev Dermatol 2009; 4:67-78.
26. Ho WY, Yeap SK, Ho CL, Rahim RA, Alitheen NB. Development of multicellular tumor spheroid (MCTS) culture from breast cancer cell and a high throughput screeningmethod using the MTTassay. PLoSONE2012; 7:e44640.
27. Friedrich J, Ebner R, Kunz-Schughart LA. Experimental anti-tumor therapy in 3-D: spheroids-old hat or new challenge? Int J Radiat Biol 2007;83: 849-71.
28. Thallinger C, Werzowa J, Poeppl W, Kovar FM, Pratscher B, Valent P, et al. Comparison of a treatment strategy combining CCI-779 plus DTIC versus DTIC monotreatment in human melanoma in SCID mice. J Invest Dermatol 2007;127:2411-7.
29. Singh S, Davis R, Alamanda V, Pireddu R, Pernazza D, Sebti S, et al. Rb-Raf-1 interaction disruptor RRD-251 induces apoptosis in metastatic melanoma cells and synergizes with dacarbazine. Mol Cancer Ther 2010;9: 3330-41.
30. Anvekar RA, Asciolla JJ, Lopez-Rivera E, Floros KV, Izadmehr S, Elkholi R, et al. Sensitization to the mitochondrial pathway of apoptosis augments melanoma tumor cell responses to conventional chemotherapeutic regimens. Cell Death Dis 2012;3:e420.
31. Engesaeter B, Engebraaten O, Florenes VA, Maelandsmo GM. Dacarbazine and the agonistic TRAIL receptor-2 antibody lexatumumab induce synergistic anticancer effects in melanoma. PLoS ONE 2012;7:e45492.
32. Tentori L, Lacal PM, Graziani G. Challenging resistance mechanisms to therapies for metastatic melanoma. Trends Pharmacol Sci 2013;34: 656-66.
33. Wang XK, He JH, Xu JH, Ye S, Wang F, Zhang H, et al. Afatinib enhances the efficacy of conventional chemotherapeutic agents by eradicating cancer stem-like cells. Cancer Res 2014;74:4431-45.
34. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, et al. Mutations of the BRAF gene in human cancer. Nature 2002;417:949-54.
35. Flaherty KT, Infante JR, Daud A, Gonzalez R, Kefford RF, Sosman J, et al. Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations. N Engl J Med 2012;367:1694-703.
36. Robert C, Karaszewska B, Schachter J, Rutkowski P, Mackiewicz A, Stroiakovski D, et al. Improved overall survival in melanoma with combined dabrafenib and trametinib. N Engl J Med 2015;372:30-9.
37. Wagle N, Van Allen EM, Treacy DJ, Frederick DT, Cooper ZA, Taylor-Weiner A, et al. MAP kinase pathway alterations in BRAF-mutant melanoma patients with acquired resistance to combined RAF/MEK inhibition. Cancer Discov 2014;4:61-8.
38. Kirsammer G, Strizzi L, Margaryan NV, Gilgur A, Hyser M, Atkinson J, et al. Nodal signaling promotes a tumorigenic phenotype in human breast cancer. Semin Cancer Biol 2014;29:40-50.
39. Quail DF, Zhang G, Findlay SD, Hess DA, Postovit LM. Nodal promotes invasive phenotypes via a mitogen-activated protein kinase-dependent pathway. Oncogene 2014;33:461-73.
40. Shackleton M, Quintana E, Fearon ER, Morrison SJ. Heterogeneity in cancer: cancer stem cells versus clonal evolution. Cell 2009;138:822-9.
41. Meacham CE, Morrison SJ. Tumour heterogeneity and cancer cell plasticity. Nature 2013;501:328-37.
42. Freeman SM, Abboud CN, Whartenby KA, Packman CH, Koeplin DS, Moolten FL, et al. The "bystander effect": tumor regression when a fraction of the tumor mass is genetically modified. Cancer Res 1993;53:5274-83.
43. Vallier L, Reynolds D, Pedersen RA. Nodal inhibits differentiation of human embryonic stem cells along the neuroectodermal default pathway. Dev Biol 2004;275:403-21.
44. Kruithof-de Julio M, Alvarez MJ, Galli A, Chu J, Price SM, Califano A, et al. Regulation of extra-embryonic endoderm stem cell differentiation by Nodal and Cripto signaling. Development 2011;138:3885-95.
45. Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, Gasser M, et al. Identification of cells initiating human melanomas. Nature 2008;451:345-9.
46. Grosse-Gehling P, Fargeas CA, Dittfeld C, Garbe Y, Alison MR, Corbeil D, et al. CD133 as a biomarker for putative cancer stem cells in solid tumours: limitations, problems and challenges. J Pathol 2013;229:355-78.
47. McAllister JC, Zhan Q, Weishaupt C, Hsu MY, Murphy GF. The embryonic morphogen, Nodal, is associated with channel-like structures in human malignant melanoma xenografts. J Cutan Pathol 2010;37 Suppl 1:19-25.
48. Turner NC, Reis-Filho JS. Genetic heterogeneity and cancer drug resistance. Lancet Oncol 2012;13:e178-85.
49. Chartrain M, Riond J, Stennevin A, Vandenberghe I, Gomes B, Lamant L, et al. Melanoma chemotherapy leads to the selection of ABCB5-expressing cells. PLoS ONE 2012;7:e36762.